Download Effects of reindeer browsing on tundra willow and its

Journal of Applied
Ecology 2004
41, 870– 879
Effects of reindeer browsing on tundra willow and
its associated insect herbivores
Blackwell Publishing, Ltd.
MICHAEL DEN HERDER,* RISTO VIRTANEN† and HEIKKI ROININEN‡
*Faculty of Forestry, University of Joensuu, PO Box 111, FIN-80101 Joensuu, Finland; †Department of Biology,
University of Oulu, PO Box 3000, FIN-90014 Oulu, Finland; and ‡Vantaa Research Centre, Finnish Forest Research
Institute, PO Box 18, FIN-01301 Vantaa, Finland
Summary
1. Browsing by large mammals may strongly constrain the growth and reproduction of
woody plants, and may alter the food quality and resource availability for herbivorous
insects. The response of the plants may vary between different growth stages, and the
preference of herbivores may be related to plant age. Understanding the effects of reindeer
Rangifer tarandus browsing on the growth of woody forage plants is important in formulating guidelines for reindeer grazing management, especially in low productivity
subarctic environments.
2. We studied the effects of summer browsing by reindeer on the growth and reproduction
of willow Salix phylicifolia and on the abundance of its insect herbivores, by studying
plants inside and outside exclosures over a period of 6 years.
3. The experiment was run in northern Finland and included 80 willow genets in an
area near the timberline formed by mountain birch Betula pubescens. At the beginning
of the experiment, half of the willows were cut at ground level to rejuvenate ramets.
4. Reindeer feeding was more intense on rejuvenated willow compared with old willow,
and the effects of browsing were more pronounced on rejuvenated plants.
5. Reindeer browsing reduced the height of willow by c. 50%, shoot length by c. 30%
and accelerated dieback of the shoots by c. 50%. Browsed willow produced fewer shoots,
with fewer buds and floral catkins, than unbrowsed willow. Browsing also reduced the
densities of the most common insect herbivores: leaf beetles of the genus Gonioctena
(Coleoptera: Chrysomelidae) and gall-inducing sawflies (Hymenoptera: Tenthredinidae)
belonging to the genera Phyllocolpa, Eupontania and Euura.
6. Synthesis and applications. We show that reindeer browsing in summer reduces biomass and diminishes reproductive success of willow; it also lowers the numbers of its
associated insect herbivores. Our results suggest that this effect will be most evident in
low-productivity tundra heaths where alternative forage plants, such as relatively
palatable and productive graminoids, are scarce. We advise that reindeer should be
maintained below the present levels of 2–3 reindeer km−2 to sustain the long-term persistence of important forage plants such as willow in these low productivity habitats.
Key-words: browsing, food preference, leaf beetles, plant growth, sawflies, tundra, willow
Journal of Applied Ecology (2004) 41, 870–879
Introduction
Grazing and browsing by ungulates have marked
effects on the abundance of deciduous scrubs and other
plants in tundra ecosystems (Henry & Svoboda 1994).
© 2004 British
Ecological Society
Correspondence: Michael den Herder, Faculty of Forestry,
University of Joensuu, PO Box 111, FIN-80101 Joensuu, Finland
(fax + 358 13 2513590; e-mail [email protected]).
Manseau, Huot & Crête (1996) reported higher abundance of Salix planifolia in ungrazed areas than in areas
with caribou Rangifer tarandus caribou (reindeer) grazing, noting that this willow was absent from some grazed
areas. Long-term experiments on the Fennoscandian
tundra have suggested that exclusion of grazers leads to
increased abundance of woody plants (Moen & Oksanen
1998), whereas intense summer grazing by reindeer
Rangifer t. tarandus virtually eliminates woody plants
(Olofsson et al. 2001). There are several studies from
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Effects of reindeer
browsing
© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
other ecosystems showing that wild ungulates and
domestic livestock can affect growth, plant structure
and reproduction of willow Salix spp. (Maschinski 2001;
Peinetti, Menezes & Coughenour 2001; Brookshire et al.
2002).
Ungulate browsing may cause a variety of morphological and physiological changes in plants, which
depend on browsing intensity and frequency, the
type of herbivory and the time of year when browsing
occurs (Danell, Huss-Danell & Bergström 1985; Danell,
Bergström & Edenius 1994). For instance, winter browsing by moose Alces alces may stimulate shoot growth in
the next growing season (Danell, Bergström & Edenius
1994; Bergman 2002), while leaf-stripping in summer
by moose or reindeer generally has the opposite effect
(Danell, Bergström & Edenius 1994). Simulated browsing experiments have shown that clipping reduced the
growth of willow Salix lanata (Ouellet, Boutin & Heard
1994), demonstrating that effects of browsing can be
particularly pronounced in low productivity habitats.
However, there are few studies showing how growth of
willow is affected when it is exposed to long-term mammal
browsing. Responses may also vary between different
plant species, growing conditions and growth stage
(Edenius, Danell & Bergström 1993). Swihart & Bryant
(2001) found that winter herbivory is heavier on mature
plants. Unfortunately, there are no experimental studies
examining the effects of summer feeding by reindeer
Rangifer tarandus L. on willow at different stages of
development. Martinsen, Driebe & Whitham (1998)
found that resprouting juvenile cottonwoods Populus
fremontii × Populus angustifolia not only had a high
nitrogen content but also contained high levels of compounds that defend against mammalian herbivores.
Similarly, Tahvanainen et al. (1985) found increased
levels of defensive compounds in juvenile willow, and
hare Lepus timidus preferred mature willow shoots to
juvenile ones. We might thus expect that reindeer would
not heavily browse resprouting juvenile willow.
It has been proposed that browsing by ungulates
affects the reproduction of plants in different ways
(Mulder 1999). Loss of foliage leads to restricted carbon
and nitrogen gain (Ouellet, Boutin & Heard 1994) and
fewer resources are left for flower production. Bergström
& Danell (1987) found that moose browsing reduced
the production of female catkins in birch Betula pendula
and Betula pubescens, and Elmqvist et al. (1987) showed
that moderately browsed willow maintained flower
production. In addition, reindeer may browse flower
buds and developing catkins. There are no detailed
studies in northern systems, but we expect reindeer to
have a negative effect on flowering and seed production
because resource limitation may prevent compensatory responses (Bryant, Chapin & Klein 1983).
The effects of browsing on the insect guild utilizing
willows can operate in several ways. Induced-chemical
responses of the plant to herbivory may change the
nutritional quality of the plant, and therefore the quality
of the plant as food (Bryant et al. 1991; Martinsen,
Driebe & Whitham 1998). Many of these induced
responses are long lasting (Bryant et al. 1991 and references therein). Browsing may reduce foliage available
for leaf-feeding insects (leaf-gallers and leaf-beetles)
and reduce buds available to bud-galling sawflies.
Alternatively, browsing may stimulate development of
long shoots, leading to increased resources for these
insects (Price 1991). Winter browsing by moose improves
the food quality for herbivorous insects, as indicated by
higher insect densities on previously browsed trees
(Danell & Huss-Danell 1985; Roininen, Price & Bryant
1997). In general, moose browsing leads to an improvement in leaf quality (Danell & Bergström 1989; Bryant
et al. 1991) and growth of longer and more vigorous
shoots (Bryant et al. 1991). For shoot- and leaf-galling
sawflies in the genera Euura and Eupontania, shoot length
has been found to correlate positively with the number
of ovipositing females and survival of the larvae (Price,
Craig & Roininen 1995; Roininen, Price & Bryant 1997),
and galls were more common on browsed trees or ramets.
Compared with the moose–woody plant–insect system,
there is little information on the reindeer–woody plant–
insect system. However, Olofsson & Strengbom (2000)
found more gall-forming insects on reindeer-browsed
willow S. lanata, even though shoot length was reduced
by leaf-stripping.
In northern Fennoscandia, Salix phylicifolia L. is
one of the common willow species browsed by reindeer
(Haukioja & Heino 1974; Nieminen & Heiskari 1989).
The objective of our study was to compare the growth
and reproductive response of S. phylicifolia to summer
browsing by reindeer. We measured several growth
characteristics inside and outside exclosures 4 and
5 years after establishment of the experiment. Furthermore, we examined the impact of reindeer feeding on
herbivorous insects on willows, in order to test the
hypothesis that summer browsing would adversely
affect both willow and its associated insect herbivores.
Materials and methods
 
The study was performed near Mt Muotkatakkavaara
(68°55′N, 20°59′E), 20 km south of the village of
Kilpisjärvi in north-western Finnish Lapland. The
area belongs to Fjeld Lapland and lies in the orohemiarctic zone (Ahti, Hämet-Ahti & Jalas 1968). Continental subalpine birch woodland is the predominant
vegetation (Hämet-Ahti 1963) below the timberline,
while treeless heath prevails at the higher altitudes
(Oksanen & Virtanen 1995). The forests are dominated
by mountain birch Betula pubescens ssp. czerepanovii
(N. I. Orlova) Hämet-Ahti. On drier sites, subarctic
heath vegetation is more frequent, dominated by Betula nana L. On moister sites thickets of willow scrub
Salix spp. are common. Here, S. phylicifolia is common,
when not subjected to flooding, while Salix lapponum
L. is dominant on sites subjected to spring flooding
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R. Virtanen &
H. Roininen
after snowmelt. In our study area, S. phylicifolia may
hybridize with Salix myrsinifolia Salisb. Phytochemical
analysis of the experimental willows has revealed
characteristics of S. myrsinifolia (P. Hallgren &
R. Julkunen-Tiitto, unpublished data).
Reindeer, which are semi-domesticated in Finland,
are the dominant large herbivores. Both wild and domestic reindeer have remarkably different summer and
winter diets. In winter, they mainly feed on terrestrial
lichens (Helle 1984; Danell et al. 1994), which they dig
up from under the snow. In summer, they feed on a wide
variety of forage plants, mainly the leaves of willow and
birch, herbs and grasses (Kelsall 1968; Haukioja &
Heino 1974; Nieminen & Heiskari 1989). The number
of reindeer managed by the Käsivarsi reindeer herders’
co-operative, to which our study area belongs, decreased
between 1994 and 1998 from 7609 to 7489 animals
(c. 1·6 reindeer km−2) (Kumpula et al. 1997; Kumpula,
Colpaert & Nieminen 1999). However, the local reindeer
owner has maintained an above-average stocking rate
of approximately 2–3 animals km−2. Willow grouse
Lagopus lagopus L. is fairly common in the study area
and may show large fluctuations in population density.
The last peak population density occurred during the
winter of 1995–96 (R. Virtanen & H. Roininen, personal
observations). Mountain hare Lepus timidus L. populations vary and occasionally they can be abundant.
However, during the period of this study hare densities
were very low. Moose Alces alces L. are important browsers, feeding on woody plants year round (Cederlund et al.
1980). However, moose are uncommon in the study area,
although they occasionally migrate through it.
The most common folivorous insects are leaf beetles
(Coleoptera: Chrysomelidae) belonging to the genus
Gonioctena Chevrolat. There were three gall-inducing
sawflies (Hymenoptera: Tenthredinidae) on our experimental plants: a leaf-folder belonging to the genus Phyllocolpa Benson, the leaf-galler Eupontania arcticornis
Konow and the bud-galler Euura mucronata Hartig.
 
© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
In the study area, 20 blocks with four willow genets in
each were established in 1997 – 98 on two sites of similar
habitat type (10 blocks in each). The two sites were
2 km apart and there was a small altitudinal difference
(±10 m) between sites. In each block of four willow
genets, two randomly chosen genets were cut at ground
level in 1997 to stimulate vegetative growth (young),
and the remaining two genets were left without any
pre-treatment (old). In each block, one of the young and
one of the old willow genets were fenced, protecting a
single willow genet from browsing, while the unfenced
willows were open for browsing. The fences measured
2 × 2 m square and 2 m in height and were constructed
from commercially available reindeer fence attached to
four fence posts. The fences did not prevent access by
insects, small mammals (such as Microtus and Clethrionomys voles and lemmings Lemmus lemmus) or willow
grouse. Consequently, each block consisted of four subplots with different treatments: Young/fenced, young/
open to reindeer and old/fenced, old/open to reindeer.
Plants that were cut at ground level in 1997 started
rejuvenating by forming new basal sprouts in 1998 and
are hereafter referred to as rejuvenated. Plants that
remained untouched are hereafter referred to as old. In
each fenced or open plot, four ramets belonging to the
same genet were selected at random and permanently
identified with a long-lasting tag. All measurements
were taken on these ramets throughout the study period.
      
Effects of reindeer summer browsing on willows were
examined from spring 2001 to early autumn 2002. We
measured the height of marked ramets in late August to
early September 2001 and 2002. Plants were measured
at the end of the growing season prior to leaf-fall, so
representing maximum annual growth. During the
same period, we measured the length of the leading
shoots to quantify the growth of the main stem of the
plant. In willow, annual internodes are clearly visible.
By measuring the distance between the internodes, we
were able to measure the annual shoot lengths back to
1998. Some parts of the shoots may not survive until
the next year and show dieback due to severe frost,
drought, disease or herbivores. In 2001, we measured
the dieback of the annual shoots back to 1998. In 2002,
we measured the dieback of the shoots grown in 2001.
Based on these measurements, we were able to reconstruct the development of the height of the plants from
1997 onwards. Furthermore, we counted the number of
shoots, the number of buds per shoot and the number
of leaves eaten by reindeer per shoot. Reindeer feed on
the leaves of willow throughout the growing season and
leave characteristic marks as a consequence of their
tendency to rip off the leaves. According to our own
observations, utilization of willows was highest in
August and had stopped almost completely by the date
the measurements were initiated.
To give an estimate of the feeding by folivorous
insects, we used a herbivory index. Each leaf of the
three leading shoots was given an index number based
on the proportion of leaf area removed by insects. Index
numbers ranged from 0 to 4, where 0 = no damage,
1 = 0–1%, 2 = 1–5%, 3 = 5–25% and 4 = 25–100% of
the leaf area eaten by insects. By calculating the mean
herbivory index of the three leading shoots, we could
give a mean herbivory index number for the whole ramet.
We also counted the number of Gonioctena spp. on ramets
in 2001. In 2001 and 2002, we counted the number of
galls of three different sawfly species: Phyllocolpa spp.,
Eupontania arcticornis and Euura mucronata.
In 2001 and 2002, we took measurements on the
reproductive capacity of the marked ramets to assess
the response to herbivory. In the third week of June, we
counted the number of catkins on each ramet as a
measure of plant reproduction.
873
Effects of reindeer
browsing
© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
 
We tested the effects of reindeer exclusion on willow
growth, reproduction and insect herbivory using repeated
measures analysis of variance (). We used habitat (site), block, browsing (fenced vs. open to reindeer)
and rejuvenation (rejuvenated plants vs. old plants) as
factors and year as the within-subject variable (SPSS
version 10·0; Anonymous 1999). Because the numbers
of leaves eaten by reindeer were counted in open plots
only, the preference of reindeer for rejuvenated or old
plants was analysed with repeated measures analysis of
variance () using habitat, block and rejuvenation as factors and year as the within-subject variable.
For all the variables there was no significant effect for
the factors block and habitat, indicating that growth
responses of the willows were more or less uniform
and independent of any small variation in the landscape.
Analyses were carried out in the univariate mode.
Mauchly’s test for sphericity was used to detect any
violations against this assumption (Potvin, Lechowicz
& Tardif 1990). This test was significant on a few occasions and where necessary Huynh–Feldt corrected degrees
of freedom were used. Analyses were conducted using
genet means from four ramets for each treatment (n = 10
for each browsing and rejuvenation treatment) rather
than individual plants. Shoot length and height data
were transformed with a natural logarithm + 1 to improve
the homogeneity of variances. The proportion of available leaves eaten by reindeer was arcsine transformed.
To test whether browsing, the growth stage of willows or sampling year had effects on the occurrence
of insects on the plants, generalized linear interactive
modelling was used. A model was constructed where the
number of counted observations in four ramets was the
response variable, and browsing (with levels fenced vs.
open), growth stage of the willow (rejuvenated vs. old)
and year (2001 vs. 2002) were explanatory variables
(factors with all their interaction terms in the initial
model). The response variable contained counts of items
and the data included many zeroes. Thus, it was assumed
that a Poisson-error structure would best approximate
the distribution of the response variable. In addition,
log-link is appropriate when dealing with positive
integer values. To take overdispersion into account, a
‘quasi-Poisson’ error structure was used in final modelling. The quasi-Poisson family differs from the Poisson
families only in that the dispersion parameter is not
fixed at 1, allowing the modelling of overdispersion
(McCullagh & Nelder 1989). Although the distributions
of residuals revealed that the data had many rather
extreme values, the residuals’ distributions appeared
satisfactory. Similar models were constructed for the
leaf-galling sawflies Phyllocolpa spp. and Eupontania
arcticornis, the bud-galling sawfly Euura mucronata
and also Gonioctena spp. Significance of explanatory
variables was tested by deletion (F-tests), starting from
the higher order interaction terms. Non-significant terms
were removed so that the minimum adequate model
Fig. 1. Feeding intensity on rejuvenated and old bushes of
Salix phylicifolia expressed as the proportion of available
leaves eaten by reindeer. Error bars are one standard error.
Rejuvenated bushes (filled bars) were cut at ground level in
1997 and old bushes (open bars) had no pre-treatment.
contained only significant explanatory variables. Analyses
were run using  version 1·6·1 (Crawley 2002).
Results
 
Reindeer ate a higher proportion of available leaves from
young rejuvenated bushes compared with old bushes (F1,19
= 6·48, P = 0·02; Fig. 1). Furthermore, in 2002 the feeding
intensity was lower than in 2001 (F1,19 = 14·24, P = 0·001).
We did not observe any damage from mountain hare.
      

The height of the willows increased significantly during
the study period (F4·6,178·9* = 432·74, P < 0·001; *Huynh–
Feldt corrected degrees of freedom; Fig. 2). In addition,
there were large differences in height between fenced
plots and plots open to reindeer (F1,39 = 13·62, P = 0·001).
A significant year × browsing interaction indicated that
the effect of fencing increased over time due to continued
willow growth in fenced plots (F4·6,178·9* = 10·47, P < 0·001).
At the start of the experiment in 1997, the mean height
of rejuvenated plants was lower and there was no difference in the height of willows inside and outside exclosures. From 1997 to 2002, reindeer exclusion resulted in
a large increase in height of rejuvenated plants (significant
browsing × rejuvenation interaction, F1,39 = 7·19, P =
0·011), and in 2002 rejuvenated plants reached the same
height as the old plants. In contrast, rejuvenated plants
not protected against reindeer browsing showed a height
increase of less than half of that of the fenced plants.
Shoot length decreased significantly during the study
period (F4,144 = 195·12, P < 0·001; Fig. 3a) and there was
a significant difference in shoot length between fenced
and open plots (F1,36 = 23·33, P < 0·001). Initially, rejuvenated plants had much longer annual shoots compared
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M. den Herder,
R. Virtanen &
H. Roininen
Fig. 2. Mean height of willows inside and outside fenced
areas with different rejuvenation treatments (rejuvenated vs.
old bushes). Error bars are one standard error. Differences
between plant heights inside and outside the fenced areas were
not significantly different in 1997, but were different for all
subsequent years.
© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
Fig. 3. (a) Current annual shoot length, (b) dieback and (c)
number of new shoots of the leading shoot of willows inside
and outside fenced areas with different rejuvenation treatments.
with old plants (F1,36 = 148·96, P < 0·001). A significant
year × browsing interaction (F4,144 = 2·71, P < 0·032)
indicated that the initially large effect of browsing
(i.e. in 1998 – 99) on shoot length levelled off with
increasing age of the plants (i.e. in 2000–02).
With decreasing shoot length, dieback of the leading
shoot decreased equally over time (F3,117 = 22·87, P < 0·001;
Fig. 3b). Furthermore, reindeer browsing increased dieback of the shoots (F1,39 = 17·06, P < 0·001). More specifically, a significant browsing × rejuvenation interaction
suggested that rejuvenated plants showed much greater
dieback compared with old plants (F1,39 = 12·5, P = 0·001).
The number of shoots emanating from the previous
year’s leading shoot increased from 1999 to 2000, and
decreased from 2000 to 2001 (F2,78 = 28·11, P < 0·001;
Fig. 3c). Reindeer browsing decreased branching (F1,39
= 42·25, P < 0·001) and the leading shoots of rejuvenated
plants produced significantly more newly grown shoots
(F1,39 = 16·1, P < 0·001). A significant year × browsing
interaction (F2,78 = 5·06, P = 0·009) suggested that the
effect of reindeer browsing on branching increased during the period 1999–2001. A browsing × rejuvenation
interaction approaching significance (F1,39 = 3·951, P
< 0·054) suggested that rejuvenated willows protected
from browsing supported more branches than those
browsed by reindeer.
Reindeer browsing markedly decreased the number
of buds per shoot (F1,39 = 11·03, P = 0·002) and rejuvenated plants had significantly more buds per shoot (F1,39 =
11·26, P = 0·002; Fig. 4a). However, the initial difference
Fig. 4. (a) The mean number of buds of the leading shoot and
(b) the mean number of catkins per ramet of willows inside
and outside fenced areas with different rejuvenation treatments.
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Effects of reindeer
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Fig. 5. Herbivory index to express the amount of defoliation
by folivorous insects of willows inside and outside fenced
areas with different rejuvenation treatments. Each leaf of the
three leading shoots was given an index number based on the
proportion of leaf area removed by insects. Index numbers
ranged from 0 to 4 where 0 = no damage, 1 = 0 –1%, 2 = 1–
5%, 3 = 5 –25% and 4 = 25 –100% of the leaf area eaten by
insects. Herbivory index numbers are based on the means for
the whole ramet.
Fig. 6. The number of leaf beetles Gonioctena spp. per ramet
of willows inside (filled bars) and outside fenced areas (open
bars) with different rejuvenation treatments.
in 2001 between browsed and open plots levelled off in
2002 (year × browsing, F1,39 = 13·06, P = 0·001).
Flowering decreased during the period 2001–02
(F1,39 = 5·07, P < 0·03; Fig. 4b). Reindeer browsing also
significantly decreased the number of catkins per ramet
(F1,39 = 20·65, P < 0·001). Old ramets had more catkins
compared with rejuvenated ramets (F1,39 = 14·18, P =
0·001) and hardly any rejuvenated bushes that were
browsed by reindeer flowered.
   
© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
We found no difference in the amount of defoliation by
folivorous insects between fenced blocks and blocks
browsed by reindeer or between rejuvenated and old
bushes (Fig. 5). There was, however, a great spatiotemporal variation in insect herbivory. From 2001 to
2002 the amount of insect-feeding on willows increased
markedly (F1,39 = 51·58, P < 0·001) and there was considerable variation between different habitats and blocks.
In 2001, there were fewer Gonioctena leaf beetles on
browsed willows (F1,79 = 7·34, P = 0·008) and there was
no significant difference between rejuvenated and old
bushes (Fig. 6). The number of Eupontania arcticornis
galls was much higher in 2001 than in 2002 (F1,157 =
12·64, P < 0·001) and also decreased strongly through
reindeer browsing (F1,157 = 14·44, P < 0·001; Fig. 7a).
The number of Phyllocolpa galls was higher on old
willows (F1,155 = 7·03, P = 0·008; Fig. 7b). A significant
interaction term for year × browsing showed that the
effect of browsing differed between the 2 years (F1,156 = 4·62,
P = 0·033). Nevertheless, browsing reduced the number
of Phyllocolpa, as indicated by a significant main effect
for browsing (parameter estimate t = 2·74, P = 0·007).
There were more Euura mucronata galls in 2002 than in
Fig. 7. The number of sawfly galls per ramet of willows
inside and outside fenced areas with different rejuvenation
treatments. There was (a) one leaf-galler Eupontania arcticornis,
( b) one leaf-folder Phyllocolpa spp. and (c) the bud-galler
Euura mucronata.
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M. den Herder,
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H. Roininen
2001 (F1,158 = 8·48, P = 0·004; Fig. 7c). Furthermore,
browsed willows had fewer Euura mucronata galls than
those in the exclosures (F1,158 = 9·87, P = 0·002).
Discussion
      

© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
This experimental study, spanning several years,
showed that browsing by reindeer strongly affects
willow growth and reproduction, as well as densities of
herbivorous insects utilizing willows. A major implication
of this study is that browsing by large mammals reduces
the abundance and performance of their food plants in
northern ecosystems. This also implies that compensatory
responses of plants are not sufficient to replace biomass
losses, contrasting with evidence from more southerly
ecosystems (Danell & Huss-Danell 1985; Danell, HussDanell & Bergström 1985; Bergström & Danell 1987;
Oba, Mengistu & Stenseth 2000).
An important result was that the effects of reindeer
browsing depended on the developmental stage of willows. Reindeer feeding was more severe on rejuvenated
willows, and the growth and survival of these juvenile
plants was significantly more affected by browsing than
non-rejuvenated old plants. To our knowledge this is
one of the few experimental demonstrations that frequent and heavy browsing on juvenile willows results in
strong dieback of browsed shoots and a reduction in
height growth (Peinetti, Menezes & Coughenour 2001).
In general, mammalian herbivores select their food on
the basis of its quality and quantity (Ball, Danell &
Sunesson 2000). Heavy reindeer feeding on rejuvenated
willow suggests that vigorous growth, possibly associated
with higher nutritional value (Martinsen, Driebe &
Whitham 1998), may prevail over the deterring effects
of increased levels of secondary compounds (JulkunenTiitto 1989; Ruuhola et al. 2001).
It is obvious that the effects of winter and summer
browsing differ. It could be that summer browsing on
leaves has more detrimental consequences for the
plants compared with pruning of shoots in winter. For
instance, Bergman (2002) found that simulated winter
browsing on Salix caprea by artificial tearing with a
moose jaw and added moose saliva led to an increase in
the number of branches. Moreover, Bergström & Danell
(1987) and Bryant et al. (1991) demonstrated that winter
browsing releases apical dominance and reduces the
competition among growing points for nutrients, which
results in enhanced shoot growth, an increased frequency of branched shoots and a higher number of
buds. In a recent study in a riparian mountain habitat,
Peinetti, Menezes & Coughenour (2001) not only found
that winter and summer browsing by elk Cervus elaphus
on Salix monticola decreased the number of shoots, but
also reported that browsed willows produced longer
and thicker shoots. In contrast, our results showed that
reindeer browsing both decreased the number of willow
shoots and reduced their length. We found no evidence
of compensatory responses, where summer browsing
would stimulate shoot production. Therefore, in this
kind of low productivity habitat, the growth of S. phylicifolia is strongly constrained by heavy repeated
browsing. The timing of browsing could be important,
as leaf-stripping in summer and browsing of shoots
and twigs in winter apparently have different effects on
plant growth and chemistry. In contrast to winter
browsing, which may release apical dominance, ripping
of leaves during the growing season directly affects the
photosynthetic capacity of the plant.
The flowering data for the 2 years of observation
suggest that reindeer browsing may reduce the reproductive output of willow. A similar reduction in flower
numbers of browsed plants in the year preceding this
study was reported by Pajunen (2001). In our experiment,
rejuvenated bushes browsed by reindeer hardly flowered,
while rejuvenated bushes protected from reindeer
flowered as much or even more than old protected bushes.
Peinetti, Menezes & Coughenour (2001) found similar
results on elk browsing on S. monticola, and Maschinski
(2001) and Brookshire et al. (2002) found that the combined effects of wild ungulates and livestock totally prevented Salix arizonica, Salix boothii and Salix geyeriana
from flowering. The latter also observed a threshold
height of 70 cm, below which willows did not flower.
Old bushes seemed to be less affected, probably because
they have been less intensively browsed for a longer
time and hence their stored energy reserves are greater.
It is still doubtful whether decreased reproductive output affects the persistence of willow. den Herder &
Niemelä (2003) showed that immigrant S. phylicifolia
seeds germinate even under heavy reindeer browsing
pressure. It is possible that willow establishment is
microsite limited, i.e. trampling, drought, poor nutrient
availability and a dense layer of scrubs and dwarf scrubs
may significantly limit seedling establishment.
      

There is growing interest in how browsers might affect
abundances of other herbivores feeding on the same
target plant, but there are few studies presenting data
from well-replicated experiments. The outcome from
this experiment was surprisingly clear: browsing by
reindeer had consistent negative effects on the densities
of galling and leaf-feeding insects. This is surprising
because most studies on comparable systems suggest
that browsing has a positive effect on insect densities
(Danell & Huss-Danell 1985; Roininen, Price & Bryant
1997). Olofsson & Strengbom (2000) showed more
galling insects on reindeer-browsed S. lanata, even
though browsing reduced the shoot length. However,
in their study browsed plants contained higher nitrogen
as an effect of reindeer urine and faeces. We cannot
explain why browsing reduced insect abundance in our
study, but we suspect that a severe loss of plant foliage
877
Effects of reindeer
browsing
and vigour, coupled with changes in foliage chemistry,
are involved (P. Hallgren & R. Julkunen-Tiitto, unpublished data). We suggest that under extreme summer
browsing, levels of photosynthesis might be so much
reduced that nitrogen uptake or its transportation to
the leaves is hindered, in contrast to situations in more
productive habitats (Peinetti, Menezes & Coughenour
2001). Our results are in line with those of Bailey &
Whitham (2003), who found that elk browsing reduced
average leaf area in aspen and thereby reduced sawfly
gall abundance, such that 90% of the galls were found
on unbrowsed aspen ramets.
The herbivory index (Fig. 5) suggests that there were
no differences in the preference of Gonioctena beetles to
browsed or rejuvenated willows. Contrary to our results,
previous studies showed a preference of herbivorous
insects for browsed trees (Danell & Huss-Danell 1985;
Roininen, Price & Bryant 1997). This also contrasts
with the results of Ikonen (2002), who found that four
leaf beetle species preferred leaves of young S. phylicifolia
plants, despite higher contents of defensive secondary
compounds. Such positive effects are mostly attributed
to increased leaf size, leaf nitrogen, shoot length and
overall plant vigour (Danell & Huss-Danell 1985; Price
1991; Price, Craig & Roininen 1995; Roininen, Price &
Bryant 1997; Ikonen 2002).
   

© 2004 British
Ecological Society,
Journal of Applied
Ecology, 41,
870–879
If reindeer management allows high densities of
reindeer, this may lead to a reduction of summer forage
in unproductive nutrient-poor habitats. Our data show
that growth, number of new shoots and reproduction
of willows are severely limited by heavy reindeer browsing. With 2–3 reindeer km−2, our study area was more
heavily browsed than other areas belonging to the
neighbouring reindeer herders’ co-operative, where
the average stocking rate was maintained at c. 1·6
reindeer km−2. Intense grazing and browsing may lead
to changes in vegetation patterns (Leader-Williams,
Smith & Rothery 1987; Oksanen, Moen & Helle 1995;
Suominen & Olofsson 2000; Augustine & McNaughton
2004) and, in the worst case, a loss of productivity of
the most preferred food plants. Preferred food plants
may eventually become replaced by less preferred food
plants (e.g. ericoids) and may become less abundant. It
seems unlikely that heavy grazing can actually increase
plant community productivity by turning a low productive tundra heath into more productive tundra dominated
by graminoids, as observed, for example, by Olofsson
et al. (2001). Instead, heavy browsing would probably
lead to a transition from relatively productive willow–
scrub to a low productive tundra heath dominated by
Betula nana and ericaceous scrub. Manseau, Huot &
Crête (1996) observed similar negative effects on plant
community productivity when caribou browsing led to
a persistent decrease in the carrying capacity of their
summer range. One year later, heavily browsed Betula
glandulosa stands within the same summer range did
not show signs of vigorous and rapid recovery after
release from heavy caribou browsing (Crête & Doucet
1998). In their regional survey, Kumpula, Colpaert &
Nieminen (1999) found that our study site belongs to
the area with the lowest summer food resources per
hectare and per reindeer in Lapland. The amount of
summer pasture available per reindeer, as well as the
quantity and quality of food, are known to affect the
growth, condition, autumn weights and productivity
of caribou and reindeer (Huot 1989; Crête & Huot
1993). The effects of heavy summer browsing may also
have cascade effects on other members of the food web.
For instance, reindeer browsing may reduce the food
resources of willow grouse (Pajunen 2001). To optimize
reindeer husbandry in a sustainable way, the growth
responses of their food plants need to be understood.
This is particularly important under the extremely harsh
and unfavourable climatic conditions that prevail in
northernmost Fennoscandia. We therefore suggest
that, in these low productivity tundra habitats where
graminoids are not abundant and where willow is an
important summer food resource, the number of reindeer
should be maintained at low levels in order to allow the
long-term persistence of willow.
Acknowledgements
We thank Kilpisjärvi Biological Station for providing
excellent lodging during the fieldwork. We also thank
Jorma Tahvanainen and Pekka Niemelä for giving
valuable advice, two anonymous referees for useful
comments, and Chris Green for linguistic revision.
Michael den Herder was supported by a grant from the
Maj and Tor Nessling Foundation, the Faculty of
Forestry of the University of Joensuu and a grant by
the Academy of Finland to Pekka Niemelä (Finnish
Centre of Excellence Programme 2002–2005, project
no. 64308). Risto Virtanen was financially supported
by the Finnish Cultural Foundation (Regional Fund of
Lapland) and Heikki Roininen by the Research Council
for Biosciences and Environment of the Academy of
Finland (project no. 47574).
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Received 26 May 2003; final copy received 11 June 2004